In silico study of kinetochore control, amplification, and inhibition effects in MCC assembly

BioSystems

Volumn 95, Issue 1, 2009, Pages 35-50

  Ibrahim, Bashar ^a,b   Schmitt, Eberhard ^c   Dittrich, Peter ^a,b   Diekmann, Stephan ^c  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b Jena Centre for Bioinformatics (JCB)   (Germany)

^c FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

MSAC; Bub3; BubR1; Cdc20; Dynamical model; Kinetochore dependent model KDM; Mad2; MCC; Template model

Indexed keywords

ANAPHASE PROMOTING COMPLEX; BUB1 RELATED PROTEIN; BUB3 PROTEIN; CELL CYCLE PROTEIN 20; PROTEIN MAD2;

INHIBITION; KARYOLOGY; MODELING;

ANAPHASE; ARTICLE; CENTROMERE; CHROMOSOME REARRANGEMENT; CHROMOSOME SEGREGATION; COMPUTER MODEL; EUKARYOTE; INHIBITION KINETICS; MATHEMATICAL MODEL; METAPHASE; MITOSIS; MITOSIS SPINDLE; MITOTIC CHECKPOINT COMPLEX; MOLECULAR MODEL; NONHUMAN; PHASE TRANSITION; QUANTITATIVE ANALYSIS; REACTION ANALYSIS; SPINDLE ASSEMBLY CHECKPOINT;

EUKARYOTA;

EID: 56849122193     PISSN: 03032647     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biosystems.2008.06.007     Document Type: Article

References (86)

1. Acquaviva C., Herzog F., Kraft C., and Pines J. The anaphase promoting complex/cyclosome is recruited to centromeres by the spindle assembly checkpoint. Nat. Cell Biol. 6 9 (2004) 892-898
2. Bolanos-Garcia V.M., Beaufils S., Renault A., Grossmann J.G., Brewerton S., Lee M., Venkitaraman A., and Blundell T.L. The conserved N-terminal region of the mitotic checkpoint protein BUBR1: a putative TPR motif of high surface activity. Biophys. J. 89 4 (2005) 2640-2649
3. Braunstein I., Miniowitz S., Moshe Y., and Hershko A. Inhibitory factors associated with anaphase-promoting complex/cylosome in mitotic checkpoint. Proc. Natl. Acad. Sci. U.S.A. 104 12 (2007) 4870-4875
4. Burton J.L., and Solomon M.J. Mad3p, a pseudosubstrate inhibitor of APCCdc20 in the spindle assembly checkpoint. Genes Dev. 21 6 (2007) 655-667
5. Campbell M.S., Chan G.K., and Yen T.J. Mitotic checkpoint proteins HsMAD1 and HsMAD2 are associated with nuclear pore complexes in interphase. J. Cell. Sci. 114 Pt 5 (2001) 953-963
6. Chan G.K., Schaar B.T., and Yen T.J. Characterization of the kinetochore binding domain of CENP-E reveals interactions with the kinetochore proteins CENP-F and hBUBR1. J. Cell Biol. 143 1 (1998) 49-63
7. Chan G.K., and Yen T.J. The mitotic checkpoint: a signaling pathway that allows a single unattached kinetochore to inhibit mitotic exit. Prog. Cell Cycle Res. 5 (2003) 431-439
8. Chen R.-H. BubR1 is essential for kinetochore localization of other spindle checkpoint proteins and its phosphorylation requires Mad1. J. Cell Biol. 158 3 (2002) 487-496
9. Chung E., and Chen R.-H. Spindle checkpoint requires Mad1-bound and Mad1-free Mad2. Mol. Biol. Cell 13 5 (2002) 1501-1511
10. Chung E., and Chen R.-H. Phosphorylation of Cdc20 is required for its inhibition by the spindle checkpoint. Nat. Cell Biol. 5 (2003) 748-753
11. Cleveland D.W., Mao Y., and Sullivan K.F. Centromeres and kinetochores from epigenetics to mitotic checkpoint signaling. Cell 112 4 (2003) 407-421
12. Compton D.A. Chromosomes walk the line. Nat. Cell Biol. 8 4 (2006) 308-310
13. D'Angiolella V., Mari C., Nocera D., Rametti L., and Grieco D. The spindle checkpoint requires cyclin-dependent kinase activity. Genes Dev. 17 20 (2003) 2520-2525
14. Davenport J., Harris L.D., and Goorha R. Spindle checkpoint function requires Mad2-dependent Cdc20 binding to the Mad3 homology domain of BubR1. Exp. Cell Res. 312 10 (2006) 1831-1842
15. DeAntoni A., Pearson C.G., Cimini D., Canman J.C., Sala V., Nezi L., Mapelli M., Sironi L., Faretta M., Salmon E.D., and Musacchio A. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr. Biol. 15 3 (2005) 214-225
16. Ditchfield C., Johnson V.L., Tighe A., Ellston R., Haworth C., Johnson T., Mortlock A., Keen N., and Taylor S.S. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161 April (2) (2003) 267-280
17. Doncic A., Ben-Jacob E., and Barkai N. Evaluating putative mechanisms of the mitotic spindle checkpoint. Proc. Natl. Acad. Sci. U.S.A. 102 18 (2005) 6332-6337
18. Doncic, A., Ben-Jacob, E., Barkai, N., 2006. Noise resistance in the spindle assembly checkpoint. Mol. Syst. Biol. 2, doi:10.1038/msb4100070.
19. Dube P., Herzog F., Gieffers C., Sander B., Riedel D., Müller S.A., Engel A., Peters J.-M., and Stark H. Localization of the coactivator Cdh1 and the cullin subunit Apc2 in a cryo-electron microscopy model of the vertebrate APC/C. Mol. Cell 20 (2005) 867-879
20. Fang G. Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol. Biol. Cell 13 3 (2002) 755-766
21. Fang G., Yu H., and Kirschner M.W. The checkpoint protein Mad2 and the mitotic regulator Cdc20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev. 12 April (12) (1998) 1871-1883
22. Fraschini R., Beretta A., Sironi L., Musacchio A., Lucchini G., and Piatti S. Bub3 interaction with Mad2, Mad3 and Cdc20 is mediated by WD40 repeats and does not require intact kinetochores. EMBO J. 20 23 (2001) 6648-6659
23. Gupta A., Inaba S., Wong O.K., Fang G., and Liu J. Breast cancer-specific gene 1 interacts with the mitotic checkpoint kinase BubR1. Oncogene 22 48 (2003) 7593-7599
24. Habu T., Kim S.H., Weinstein J., and Matsumoto T. Identification of a MAD2-binding protein, CMT2, and its role in mitosis. EMBO J. 21 23 (2002) 6419-6428
25. Hagan R.S., and Sorger P.K. Cell biology: the more MAD, the merrier. Nature 434 7033 (2005) 575-577
26. Hardwick K.G. Checkpoint signalling: Mad2 conformers and signal propagation. Curr. Biol. 15 4 (2005) R122-R124
27. Hardwick K.G., Johnston R.C., Smith D.L., and Murray A.W. MAD3 encodes a novel component of the spindle checkpoint which interacts with Bub3p, Cdc20p, and Mad2p. J. Cell Biol. 148 March (5) (2000) 871-882
28. Hoffman D.B., Pearson C.G., Yen T.J., Howell B.J., and Salmon E.D. Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol. Biol. Cell 12 7 (2001) 1995-2009
29. Hoops S., Sahle S., Gauges R., Lee C., Xu L., Mendes P., and Kummer U. COPASI-a complex pathway simulator. Bioinformatics 22 (2006) 3067-3074
30. Howell B.J., Hoffman D.B., Fang G., Murray A.W., and Salmon E.D. Visualization of Mad2 dynamics at kinetochores, along spindle fibers, and at spindle poles in living cells. J. Cell Biol. 150 6 (2000) 1233-1250
31. Howell B.J., Moree B., Farrar E.M., Stewart S., Fang G., and Salmon E.D. Spindle checkpoint protein dynamics at kinetochores in living cells. Curr. Biol. 14 11 (2004) 953-964
32. Hoyt M.A. A new view of the spindle checkpoint. J. Cell Biol. 154 5 (2001) 909-911
33. Hwang L.H., Lau L.F., Smith D.L., Mistrot C.A., Hardwick K.G., Hwang E.S., Amon A., and Murray A.W. Budding yeast Cdc20: a target of the spindle checkpoint. Science 279 5353 (1998) 1041-1044
34. Ibrahim B., Diekmann S., Schmitt E., and Dittrich P. In-Silico modeling of the mitotic spindle assembly checkpoint. PLoS ONE 3 February (2) (2008) e1555. http://www.plosone.org/doi/pone.0001555 http://www.plosone.org/doi/pone.0001555
35. Ibrahim B., Dittrich P., Diekmann S., and Schmitt E. Stochastic effects in a compartmental model for mitotic checkpoint regulation. J. Integr. Bioinform. 4 3 (2007)
36. Ibrahim B., Dittrich P., Diekmann S., and Schmitt E. Mad2 binding is not sufficient for complete Cdc20 sequestering in mitotic transition control (an in silico study). Biophys. Chem. 134 1-2 (2008) 93-100
37. Jeganathan K.B., and van Deursen J.M. Differential mitotic checkpoint protein requirements in somatic and germ cells. Biochem. Soc. Trans. 34 Pt 4 (2006) 583-586
38. Kallio M.J., Beardmore V.A., Weinstein J., and Gorbsky G.J. Rapid microtubule-independent dynamics of Cdc20 at kinetochores and centrosomes in mammalian cells. J. Cell Biol. 158 5 (2002) 841-847
39. Kim M., and Kao G.D. Newly identified roles for an old guardian: profound deficiency of the mitotic spindle checkpoint protein BubR1 leads to early aging and infertility. Cancer Biol. Ther. 4 2 (2005) 164-165
40. King E.M.J., van der Sar S.J.A., and Hardwick K.G. Mad3 KEN boxes mediate both Cdc20 and Mad3 turnover, and are critical for the spindle checkpoint. PLoS ONE 2 (2007) e342
41. Kops G.J.P.L., Weaver B.A.A., and Cleveland D.W. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 5 10 (2005) 773-785
42. Lampson M.A., and Kapoor T.M. The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat. Cell Biol. 7 1 (2005) 93-98
43. Lénárt P., and Peters J.-M. Checkpoint activation: donot get mad too much. Curr. Biol. 16 June (11) (2006) 412-414
44. Luo X., Tang Z., Xia G., Wassmann K., Matsumoto T., Rizo J., and Yu H. The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat. Struct. Mol. Biol. 11 4 (2004) 338-345
45. Maiato H., DeLuca J., Salmon E.D., and Earnshaw W.C. The dynamic kinetochore-microtubule interface. J. Cell Sci. 117 (2004) 5461-5477
46. Mao Y., Abrieu A., and Cleveland D.W. Activating and silencing the mitotic checkpoint through CENP-E-dependent activation/inactivation of BubR1. Cell 114 1 (2003) 87-98
47. Mao Y., Desai A., and Cleveland D.W. Microtubule capture by CENP-E silences BubR1-dependent mitotic checkpoint signaling. J. Cell Biol. 170 6 (2005) 873-880
48. Mapelli M., Filipp F.V., Rancati G., Massimiliano L., Nezi L., Stier G., Hagan R.S., Confalonieri S., Piatti S., Sattler M., and Musacchio A. Determinants of conformational dimerization of Mad2 and its inhibition by p31comet. EMBO J. 25 6 (2006) 1273-1284
49. MATLAB, 2007. The MathWorks, Inc.-MATLAB and Simulink for Technical Computing: homepage. Retrieved June 5, 2007, from http://www.mathworks.com/.
50. May K.M., and Hardwick K.G. The spindle checkpoint. J. Cell Sci. 119 Pt 20 (2006) 4139-4142
51. Meraldi P., Draviam V.M., and Sorger P.K. Timing and checkpoints in the regulation of mitotic progression. Cell 7 July (1) (2004) 45-60
52. Millband D.N., and Hardwick K.G. Fission yeast Mad3p is required for Mad2p to inhibit the anaphase-promoting complex and localizes to kinetochores in a Bub1p-, Bub3p-, and Mph1p-dependent manner. Mol. Cell Biol. 22 8 (2002) 2728-2742
53. Minshull J., Sun H., Tonks N.K., and Murray A.W. A MAP kinase-dependent spindle assembly checkpoint in Xenopus egg extracts. Cell 79 November (3) (1994) 475-486
54. Morrow C.J., Tighe A., Johnson V.L., Scott M.I.F., Ditchfield C., and Taylor S.S. Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20. J. Cell Sci. 118 Pt 16 (2005) 3639-3652
55. Musacchio A., and Hardwick K.G. The spindle checkpoint: structural insights into dynamic signaling. Nat. Rev. Mol. Cell Biol. 3 10 (2002) 731-741
56. Musacchio A., and Salmon E.D. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8 (2007) 379-393
57. Nasmyth K. How do so few control so many?. Cell 120 6 (2005) 739-746
58. Ohi M.D., Feoktistova A., Ren L., Yip C., Cheng Y., Chen J.-S., Yoon H.-J., Wall J.S., Huang Z., Penczek P.A., Gould K.L., and Walz T. Structural organization of the anaphase-promoting complex bound to the mitotic activator Slp1. Mol. Cell 28 (2007) 871-885
59. Passmore L.A., Booth C.R., Vénien-Bryan C., Ludtke S.J., Fioretto C., Johnson L.N., Chiu W., and Barford D. Structural analysis of the anaphase-promoting complex reveals multiple active sites and insights into polyubiquitylation. Mol. Cell 20 (2005) 855-866
60. Peters J.-M. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9 5 (2002) 931-943
61. Peters J.-M. The anaphase-promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. 7 (2006) 644
62. Poddar A., Stukenberg P.T., and Burke D.J. Two complexes of spindle checkpoint proteins containing Cdc20 and Mad2 assemble during mitosis independently of the kinetochore in Saccharomyces cerevisiae. Eukaryot. Cell 4 5 (2005) 867-878
63. Popper K. Logik der Forschung. Schriften zur wissenschaftlichen Weltauffassung VI (1935), Springer Verlag, Wien
64. Rancati G., Crispo V., Lucchini G., and Piatti S. Mad3/BubR1 phosphorylation during spindle checkpoint activation depends on both Polo and Aurora kinases in budding yeast. Cell Cycle 4 7 (2005) 972-980
65. Reddy S.K., Rape M., Margansky W.A., and Kirschner M.W. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature 446 April (2007) 921-925
66. Sear R.P., and Howard M. Modeling dual pathways for the metazoan spindle assembly checkpoint. Proc. Natl. Acad. Sci. U.S.A. 103 45 (2006) 16758-16763
67. Shah J.V., Botvinick E., Bonday Z., Furnari F., Berns M., and Cleveland D.W. Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing. Curr. Biol. 14 11 (2004) 942-952
68. Shannon K.B., Canman J.C., and Salmon E.D. Mad2 and BubR1 function in a single checkpoint pathway that responds to a loss of tension. Mol. Biol. Cell 13 (2002) 3706-3719
69. Steuerwald N. Meiotic spindle checkpoints for assessment of aneuploid oocytes. Cytogenet. Genome Res. 111 3-4 (2005) 256-259
70. Stucke V.M., Baumann C., and Nigg E.A. Kinetochore localization and microtubule interaction of the human spindle checkpoint kinase Mps1. Chromosoma 113 1 (2004) 1-15
71. Stucke V.M., Sillje H.H.W., Arnaud L., and Nigg E.A. Human Mps1 kinase is required for the spindle assembly checkpoint but not for centrosome duplication. EMBO J. 21 7 (2002) 1723-1732
72. Sudakin V., Chan G.K., and Yen T.J. Checkpoint inhibition of the APC/C in hela cells is mediated by a complex of BubR1, Bub3, Cdc20, and Mad2. J. Cell Biol. 154 September (5) (2001) 925-936
73. Tang Z., Bharadwaj R., Li B., and Yu H. Mad2-independent inhibition of APCCdc20 by the mitotic checkpoint protein BubR1. Dev. Cell 1 2 (2001) 227-237
74. Taylor S.S., Ha E., and McKeon F. The human homologue of Bub3 is required for kinetochore localization of Bub1 and a Mad3/Bub1-related protein kinase. J. Cell Biol. 142 1 (1998) 1-11
75. Taylor S.S., Scott M.I.F., and Holland A.J. The spindle checkpoint: a quality control mechanism which ensures accurate chromosome segregation. Chromosome Res. 12 6 (2004) 599-616
76. Thornton B.R., Ng T.M., Matyskiela M.E., Carroll C.W., Morgan D.O., and Toczyski D.P. An architectural map of the anaphase-promoting complex. Genes Dev. 20 (2006) 449-460
77. Thornton B.R., and Toczyski D.P. Precise destruction: an emerging picture of the APC. Genes Dev. 20 (2006) 3069-3078
78. Townsley F.M., Aristarkhov A., Beck S., Hershko A., and Ruderman J.V. Dominant-negative cyclin-selective ubiquitin carrier protein E2-C/UbcH10 blocks cells in metaphase. Proc. Natl. Acad. Sci. U.S.A. 94 March (1997) 2362-2367
79. Vink M., Simonetta M., Transidico P., Ferrari K., Mapelli M., Antoni A.D., Massimiliano L., Ciliberto A., Faretta M., Salmon E.D., and Musacchio A. In vitro FRAP identifies the minimal requirements for Mad2 kinetochore dynamics. Curr. Biol. 16 8 (2006) 755-766
80. Xia G., Luo X., Habu T., Rizo J., Matsumoto T., and Yu H. Conformation-specific binding of p31(comet) antagonizes the function of Mad2 in the spindle checkpoint. EMBO J. 23 15 (2004) 3133-3143
81. Yu H. Regulation of APC-Cdc20 by the spindle checkpoint. Curr. Opin. Cell Biol. 14 6 (2002) 706-714
82. Yu H. Structural activation of Mad2 in the mitotic spindle checkpoint: the two-state Mad2 model versus the Mad2 template model. J. Cell Biol. 173 2 (2006) 153-157
83. Yu H. Cdc20: a WD40 activator for a cell cycle degradation machine. Mol. Cell 27 (2007) 3-16
84. Yu H., and Tang Z. Bub1 multitasking in mitosis. Cell Cycle 4 2 (2005) 262-265
85. Zhou Y., Ching Y.-P., Ng R.W.M., and Jin D.-Y. Differential expression, localization and activity of two alternatively spliced isoforms of human APC regulator CDH1. Biochem. J. 374 Pt 2 (2003) 349-358
86. Zhu C., Zhao J., Bibikova M., Leverson J.D., Bossy-Wetzel E., Fan J.-B., Abraham R.T., and Jiang W. Functional analysis of human microtubule-based motor proteins, the kinesins and dyneins, in mitosis/cytokinesis using RNA interference. Mol. Biol. Cell 16 7 (2005) 3187-3199